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Journal of Nanomedicine Research
Graphene Oxide for Biomedical Applications
Mini Review
Abstract
Graphene oxide (GO) is one of the most promising functional materials used in
various applications like energy storage (batteries and supercapacitors) sensors,
photocatalysis, electronics and in biomedicine. The last 10 years literature on GO for
biomedical applications revealed and confirmed the scope of its potential capabilities
as biomaterial. GO alone and its modified form with different materials (surface
functionalization, immobilization of nanoparticles and composite formation) also
proved as a multifunctional candidate for medical biotechnology. A material for its
use in biomedical applications must be biocompatible and nontoxic to the living cells..
Although there are some concerns about the toxicity of the GO in specific cases, a
dosage range and size effects reported in the literature to use it as a nontoxic materials.
In view of all these points, an effort has been made to review and emphasize the scope
of GO as a biomedical agent for the applications like targeted drug delivery, cancer
theranostics, bioimaging and biosensors etc. Further, potential applications along
with the future scope and limitations of GO have also been highlighted in this review.
Keywords: Graphene oxide; Nanocomposites; Toxicity; Biosensors; Biomedicine;
Volume 5 Issue 6 - 2017
School of Engineering Sciences and Technology, University of
Hyderabad, India
*Corresponding author: Pradip Paik, School of Engineering
Sciences and Technology, University of Hyderabad,
Telangana, India, Tel: +91-040-2313-4457 (O);
Email:
Received: June 5, 2017 | Published: July 12, 2017
Cancer; Drug delivery
Introduction
GO is mainly used in biomedicine such as for drug delivery,
cancer therapy, imaging and biosensors because of its physico
chemical properties and biocompatibiliy. GO possesses unique
structure i.e., graphene basal plane is attached with various
biocompatible functional groups like carboxylic (COOH) and
hydroxyl (OH) etc. The attached functional groups lead to further
functionalization and conjugation or immobilization of other
nanoparticles on its surface. Further, the size (number of layers,
lateral dimension) and shape of GO plays an important role in
deciding its properties that can be used in various applications.
Thickness gradient of the GO sheets showed various functionality
and tunable properties. Based on the reported literature in the
past decade, a comprehensive review on the GO’s applications in
the biomedicine has been summarized in to four main categories,
such as
a. Drug delivery and Cancer therapy.
b. Biosensors.
c. Bio-Imaging.
d. Antibacterial activities and the Toxicity effects have also
been discussed in the separate section.
Discussion
Drug delivery and cancer therapy
Research on GO nanocomposites was reported extensively
for its uses in drug delivery and cancer therapy. GO played a
significant role in sorting out the drawbacks in dealing with
cancer treatment. The extensive loading of anticancer drugs on
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GO is essentially influenced by the pi-pi stacking interactions.
A hybrid nanocomposite of Hypocrellin B (HB) stacked GO can
be synthesized through pi-pi interaction. This nanocomposite
generates reactive oxygen species (ROS) efficiently and accelerate
the killing of tumor cells under radiation [1]. Gold (Au) nanorods
vesicle@ reduced graphene oxide (rGO) hybrid nanocomposite
showed excellent drug release, enhanced photo thermal and
photo acoustic effect to treat the cancer cells when loaded with
commonly used anticancer drug doxorubicin (DOX). DOX release
can be controlled by the near infrared (NIR) photothermal effect
in intracellular acidic environment. This nanocomposite enables
efficient inhibition of tumor growth due to sequential drug release
and killing of infected cells [2].
GO on integration with NIR radiation produce heat inside
cancer cells. Further it is reported that radionuclide I-131 labeled
PEG with rGO can be used in potential combined therapies, e.g.,
photo thermal therapy (PTT) and radio therapy to treat the
cancer cells. GO on excitation with NIR radiation, induce the
photothermal effect while I-131 emits X-rays to kill the cancer
cells. Due to this multiple effects the efficient elimination of
tumor cells is possible. However, there is a concern on toxicity of
this nanocomposites [3]. A core-shell nanocomposite of chitosan
based polyseudorotaxane shell and (Fe3O4@GO@mSiO2) core
showed excellent pH dependent release. The extent of drug
release can be controlled by changing the pH and the bursting of
shell at 5.5 pH showed maximum release. Furthermore, this coreshell nanocomposite is quite soluble and formed stable colloid in
biological fluids [4]. Hydrophobic drugs can also be delivered to
the tumor cells using GO. Water insoluble anticancer drug SN38
(hydrophobic aromatic molecules including a camptothecin (CPT)
analogue) can be made soluble for treating cancer cells efficiently
J Nanomed Res 2017, 5(6): 00136
Copyright:
©2017 Santhosh et al.
Graphene Oxide for Biomedical Applications
by loading them with novel nanocomposite of nano GO with
branched polyethylene glycol (NGO@branched PEG). This drug
loaded nanocomposite formulation showed high cancer killing
potency than that of irinotecan (CPT-11) [5].
Loading of more amount of drug is possible due to the surface
functionality and high surface area of GO. As an example, more
amount of drug loading (irinotecan) was possible due to the high
surface area of GO in hyaluronic acid/polyaspartamide based
double network nanogels@GO nanostructure. This loaded drug
can be driven to the target through the changing the pH of external
medium and NIR irradiation and can be treated the human colon
cancer [6]. rGO blending with alginate@chitosan derivatives
(rGO@CSD) hydrogel is also a potential candidate for delivery
of various small drug molecules. This nanocomposite exhibited
a high drug loading efficiency of ~82.8% for small molecule
fluorescein sodium (FL) CSD/rGO/alginate and also showed
negligible cytotoxicity to hepatic stellate cell lines [7]. A thermo
sensitive nanogel of N-isopropyl acrylamide (NIPAM) modified GO
nanocomposite showed potential for high drug loading capacity
and excellent drug release behaviour at high temperature. It was
also observed that there was no burst release with temperature
[8]. Magnetically (Fe3O4) modified GO functionalized with chitosan
and methoxy poly (ethylene glycol) mPEG-NHS nanostructure
was used for targeted drug delivery of chemotherapy drugs
CPT-11 and DOX. High drug loading and pH dependent drug
release properties are promising for targeted drug delivery and
cancer therapy [9]. GO-Fe3O4 super paramagnetic drug carrier
was developed with loading of 18.6 wt% of DOX hydrochloride.
The loading capacity was as high as 1.08 mg/mg. The loaded
and unloaded nanocomposites showed good hydrophilicity.
Aggregation under acidic conditions can be regulated by applying
external magnetic fields [10]. CpG oligodeoxynucleotides (ODNs)
loading capacity was increased on GO-chitosan nanocomposites
and showed lower cytotoxity compared with GO. Loading of CpGODNs was due to the electrostatic interaction between CpG-ODNs
and GO-CS [11]. Moreover, nano GO (NGO) sheets showed lesser
cytotoxicity when they were used for drug delivery and cancer
treatment. Folic acid modified NGO loaded with dual drugs DOX
and camptothecin (CPT) showed remarkable high toxicity to
(Michigan cancer foundation-7) MCF-7 cells, while these drugs
are loaded with pristine NGO showed lesser cytotoxicity. The
loading ability of this nanostructure for multiple drugs enable us
its potential use in biomedicine [12].
Multifunctional nanocomposites have also been reported
based on the GO for drug loading, cancer treatment and imaging
etc. [mPEG]@NGO was prepared for loading of photosensitizer
zinc phthalocyanine (ZnPc) towards treating cancer cells
MCF-& through photodynamic therapy (PDT). Though ZnPc is
hydrophobic, it is internalized in MCF-7 cells with the addition of
NGO-mPEG nanocomposite [13]. Low molecular weight branched
polyethylenimine (BPEI) attached GO showed an improved DNA
binding, condensation and transfection efficiency compared
to high molecular weight BPEI. Due to the tunability of GO, this
BPEI@GO hybrid nanocomposite could be extended to SiRNA
delivery and PTT [14]. Light controllable CpG-ODNs delivery was
proposed and showed excellent photothermal and immunological
effects towards the cancer cell tumor reduction in GO@PEG and
2/6
PEI nanocomposites [15]. Through electrostatic self-assembly
of functionalized GO with chitosan and sodium alginate a
nanocomposite was formed and loaded with DOX, and showed
pH dependent drug release behavior. Remarkable inhibition of
MCF-7 cancer cells was also reported using this nanocomposite
[16]. GO@sodium alginate nanohybrid showed potential for
DOX loading and exhibited profound cytotoxicity to HeLa cells.
A very high loading capacity of 1.843 mg/mg was obtained for
this nanocomposite under the physiological conditions of pH 6.5
and 7.4 [17]. Authors of this work reported that an anticancer
effect of 13 times more than the previous study was obtained
using GO@SiO2/TiO2 nanocomposite. Multi functionality of this
nanocomposite showed potential for loading of anticancer drug
protoporphyrinIX and efficient for both PDT and PTT [18]. A
nanocomposite of rGO@phosphorescent PEG modified Ru (II)
complex (Ru-PEG) also developed and is very effective for both
PTT and PDT. This nanocomposite showed high efficacy towards
multimodal imaging and treatment of the cancer cells through the
generation of ROS [19]. GO-folic acid (FA)/bovine serum albumin
(BSA) nanocomposite loaded with DOX showed potential role in
treating the cancer cells [20].
The strategy of core-shell formation was also employed for
designing the multifunctional GO nanocomposites for drug delivery
and cancer treatment. Core-Shell nanostructure of upconversion
nanoparticles (UCNP) and GO quantum dots were synthesized and
used for imaging as well as cancer treatment. A photosensitizer
was loaded for PDT and a chemotherapy drug (hypocrellin A) was
also attached on GO quantum dots and combined with PEGlayted
UCNP. This nanostructure was multifunctional for cell imaging,
drug delivery and cancer therapy [21]. A multifunctional nano
structure consisting of fluorescein loaded zeolitic imidazolte
frameworks-8 with GO was developed for simultaneous pH
controlled drug release and PTT. This nanostructure showed
high efficacy in killing cancer cells when irradiated with 808 nm
near NIR [22]. GO@chlorogenic acid nanocomposite showed cell
viability > 80% to the normal cells and in contrary showed an
enhanced toxicity towards cancer cells (HepG2, A549 and HeLa
cells) [23]. rGO has been synthesized by hydrothermal reduction
(nontoxic) and surfactant free dispersion was obtained by
applying ultrasonication. Stable rGO dispersion was obtained by
optimizing the ultrasonic conditions and was used for an efficient
delivery of anti-cancer drug Paclitaxel [24]. A composite of nanosized graphene oxide and gold (NGO@Au) was synthesized and
GO was attached with folic acid. This nanocomposite was used for
targeting the cancer cells and simultaneous release of loaded DOX
and Au nanoparticles which substantially increased the inhibition
of cancer cells upon exposure of NIR radiations (in vivo) [25].
Biosensors
GO based sensors were developed and used for various
biological moieties detection. Especially the fluorescence
quenching nature of GO played an important role in enhancing
the sensitivity of the probe. Further, GO was used to detect
mostly DNA with low background signal. GO and silver (Ag)
ions nanocomposite was used for the detection of bacteria. The
Ag ions diffused from the composite and kill the bacteria. The
efficiency of this sensor was tested through a electrochemical
Citation: Santhosh KK, Modak MD, Paik P (2017) Graphene Oxide for Biomedical Applications. J Nanomed Res 5(6): 00136.
DOI: 10.15406/jnmr.2017.05.00136
Copyright:
©2017 Santhosh et al.
Graphene Oxide for Biomedical Applications
method and compared with conventional Dot blot assay [26]. A
nanocomposite of GO@Au nanorods was synthesized to detect
the DNA. DNA sensor based on this nanocomposite showed high
selectivity and distinguished complementary DNA sequences
from huge amount of single-base mismatched DNA (1000:1)
[27]. DNA templated click chemistry strategy based on GO was
proposed for the fluorescence detection of Cu2+. Low detection
limit was obtained under the optimal conditions. The specificity
of the click chemistry and GO quenching ability revealed low
detection limit [28].
A hydrogel of GO@fish sperm DNA was used for mitochondrial
(label-free) DNA detection by measuring the conductivity through
the impedance analysis. The conductivity of this hydrogel can be
tuned by varying the GO’s properties. Moreover, this hydrogel
electrode showed potential for the deduction of ovarian cancer
cells DNA samples [29]. DNA immobiliized on GO glassy electrode
nanocomposite was proposed for the detection of acrylamide
(AA). Due to the excellent electron transfer ability of GO, sensing
ability of this nanocomposite was linear to the concentration
of DNA [30]. Double strand DNA was directly detected without
denaturation by using peptide nucleic acid (PNA) modified
graphene oxide as a fluorescence quencher. This composite
showed very low background signal, sequence selectivity, high
sensitivity and tighter turn-on signal control [31]. There are
some reports even on adenosine triphosphate (ATP) sensing by
GO based nanocomposites. An integrated GO and hairpin shaped
molecular aptamer beacon (MAB) nanocomposite was proposed
and showed quenched fluorescence intensity in the absence of
ATP. When this nanocomposite is interacted with ATP, quenched
fluorescence intensity was recovered and low background signal
was observed [32]. Rather than physisorbed aptamer probes,
covalently linked aptamer probes (fluorophore and amino dual
modified) showed better detection of ATP. Covalently linked
aptamer probes on GO showed higher fluorescence signal when
imaging intracellular ATP [33].
Bio-imaging
GO was proved to be a potential bioimaging tool for tumor
cells. Tuning the lateral size of the GO in the nano range yields
fluorescent property to it. A luminescent single layered NGO was
developed and showed promising applications as live cell imaging
agent in the NIR and visible range with low background signal.
Moreover pi-pi stacking of anti-cancer drug (e.g., DOX) was found
suitable for killing cancer cells in vitro [34]. A nanocomposite
GO@ aptamer-carboxyfluorescein (FAM) was fascinated for
probing in living cells and this nanocomposite showed great
sensing, protecting capabilities in living cells [35].
Antibacterial activity
GO composites are also promising candidates for antibacterial
activities. Few GO-based nanocomposites evidenced better
antibacterial activities compared to the existing materials.
chitosan@AgNPs@GO nanocomposite exhibited highly efficient
antibacterial activity towards the bacteria (methicillin-resistant
Staphylococcus aureus) strains. This nanocomposite showed
better antibacterial activity than the AgNPs or GO@AgNP materials
[36]. GO- zinc oxide (ZnO) nanofillers filled poly lactic acid (PLA)
3/6
matrix nanocomposite showed multiple improved properties like
mechanical strength and antibacterial activity [37].
Toxicity
Toxicity and biocompatibility are the prior concerns for the
biomedical materials. There were various studies on the toxicity
and biocompatibility of the GOs and its derivatives. Toxicity and
in vivo biodistribution of NGO@poly sodium 4-styrenesulfonate
(PSS) nanocomposite was studied for 6 months after intravenously
injecting in mice. Potential accumulation of NGO@PSS was
observed in the lung, liver and spleen. Upon accumulation, injury
and chronic inflammation of these parts confirms the toxicity
of this nanocomposite [38]. The effect of size and concentration
of GO sheets on the cytotoxicity of normal cells and cancer cell
were elucidated. Especially low concentrations of the GO showed
negligible toxicity.
rGO was synthesized by sonication and followed by reduction
of PEGlayted GO sheets. Micron and nano sized (lateral) rGO
sheets were obtained and tested for cyto and geno toxic effects.
A high concentration of 100 mg/mL after 1 h exposure time,
cytotoxic effect was observed and this study showed the effect
of concentration of rGO cytotoxicity [39]. Toxicity of bare GO was
evaluated in male rats and observed after seven days of injection
with different concentrations of GO which causes inflammation in
lung, spleen and liver. This study proposed that low concentration
of GO is nontoxic [40]. A lower cytotoxicity was observed in the
graphene synthesized from reduction of GO using pectin from
Tithonia divesifolia [41]. GO was synthesized by unzipping
the single wall carbon nanotubes (CNT) and cytotoxicity was
examined towards human neuroblastoma cells. The cytotoxicity of
this GO was checked with SK-N-BE (2) and SH-SY5Y cell lines and
found low concentration of GO gives minimal effects on healthy
cells [42]. GO can be single layer and multilayer and the number
of layers definitely changes its physico chemical properties
and the studies were done in this regard also. Cytotoxicity of
single layered GO (SLGO) and multi layered GO (MLGO) was
investigated systematically. The dependence of size and dose of
SLGO and MLGO towards toxicity was studied in the presence /
absence of pluoronic F-127 on THP-1 cells. This study revealed
that prior consideration of GO concentration and dose need to be
optimized preceding to biomedical applications [43]. To counter
the effects of GO toxicity, it has been further functionalized and
showed no toxicity. A nontoxic and biocompatible nanostructure
of PEGlayted rGO was developed and studied with mouse bone
marrow stem cells. No increase in ROS found and confirmed by
cell function [44]. From the above information, it is clear that GO
is a potential candidate for biomedical applications and eventually
low concentration of GO is nontoxic.
Other than the above mentioned potential applications, GO
also showed mutagenesis, scaffold generation, anti-tuberculosis,
aromatic hydrocarbons extractions from food samples, glucose
sensitivity and triggered growth in plant when treated with it. In
vivo, in vitro studies of GO injected intravenously in mice showed
mutagenesis compared to the cyclophosphamide, a classic
mutagen. This study reveals an extra control needs to be taken
on the doses of the GO injection [45]. Five times enhanced growth
Citation: Santhosh KK, Modak MD, Paik P (2017) Graphene Oxide for Biomedical Applications. J Nanomed Res 5(6): 00136.
DOI: 10.15406/jnmr.2017.05.00136
Copyright:
©2017 Santhosh et al.
Graphene Oxide for Biomedical Applications
was observed with 20 mg/L of GO while untreated tobacco
roots showed lesser growth. Treating tobacco seedlings with GO
affected the gene transcript levels of the IAAA relatives allowed
enhanced root growth [46]. GO@BSA showed strong binding with
vascular endothelial growth factor (VEGF) resulting in blocking
the interaction between VEGF and their receptors which further
results in reduced/blocked blood vessel formation in rabbit.
So from this, GO can act as anti-angiogenic agent [47]. A highly
hydrophilic nanostructure of COOH groups functionalized GO
with beta-cyclodextrin was proposed and showed dispersion
stability for 12 months, which will make them applicable for
biology and medicine [48]. Graphene derived from removal
of oxygen functional groups of GO showed potential as antituberculosis agent towards M. Tuberculosis (M. TB) H37Ra [49].
Wound healing nanocomposite fibers based on GO with poly(2hydroxyethyl
methacrylate)-graft-poly(epsilon-caprolactone)
[P(HEMA-g-CL)] was proposed and showed in vitro degradability,
hydrophilicity, conductivity and biocompatibility towards
application as nano scaffolds for regenerative medicine [50].
Peptide (arginine-glycine-aspartic acid) modified GO showed
better biocompatibility than the pristine GO. At the same time,
AMP (Antimicrobial peptide modified Go showed potential for
sterilization [51]. 16 polycyclic aromatic hydrocarbons (PAHs)
were extracted from vegetable oil by using nanocomposite
of 3D ionic liquid functionalized magnetic GO. Compared to
existing molecularly imprinted solid phase extraction method
(MSPE), MSPE based on this nanocomposite is cost effective and
efficient for light PAHs extraction [52]. GO-BSA nanocomposite
hydrogel showed better pH glucose sensitivity and lower initial
burst release compared to HTCC/BSA and HTCC/2.0wMGO-BSA
hydrogels [53]. PEGlayted GO-hemin composite showed higher
peroxidase like activity than bare PEG@GO composite [54].
Conclusion
GO’s potential applications in the field of biomedicine have
been revealed based on the reported works in the past few
years. GO’s structure, size and shape played an important role
in various applications. Because of the high surface area a large
number of nanoparticles or biomolecules were immobilized on
it that together lead to multifunctional nanocomposites. The size
reduction of GO yielded it to be a fluorescence bio marker. The
various functional groups attached to GO increase its dispersity
in various bio fluids. Additionally, hydrophobic drug loaded GO
can easily be delivered into the cancer cells for enhancing the
efficiency of treatment. Though there are some concerns about
GO’s cytotoxicity, the tunability of the size and dose made this
material nontoxic and biocompatible. These findings in the
literature enable one to recognize and use GO’s tremendous
applicability in biomedicine. However, there is still a lot of scope
to elevate its potential. Studies based on the GO functionalized
with single type of oxygen functional group for different cancer
cells should be focused and it can be further checked with other
oxygen moiety to the different cancer cells.
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Citation: Santhosh KK, Modak MD, Paik P (2017) Graphene Oxide for Biomedical Applications. J Nanomed Res 5(6): 00136.
DOI: 10.15406/jnmr.2017.05.00136
Copyright:
©2017 Santhosh et al.
Graphene Oxide for Biomedical Applications
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Citation: Santhosh KK, Modak MD, Paik P (2017) Graphene Oxide for Biomedical Applications. J Nanomed Res 5(6): 00136.
DOI: 10.15406/jnmr.2017.05.00136